Abstract
BackgroundFundamental for understanding the evolution of communication systems is both the variation in a signal and how this affects the behavior of receivers, as well as variation in preference functions of receivers, and how this affects the variability of the signal. However, individual differences in female preference functions and their proximate causation have rarely been studied.Methodology/Principal FindingsCalling songs of male field crickets represent secondary sexual characters and are subject to sexual selection by female choice. Following predictions from the “matched filter hypothesis” we studied the tuning of an identified interneuron in a field cricket, known for its function in phonotaxis, and correlated this with the preference of the same females in two-choice trials. Females vary in their neuronal frequency tuning, which strongly predicts the preference in a choice situation between two songs differing in carrier frequency. A second “matched filter” exists in directional hearing, where reliable cues for sound localization occur only in a narrow frequency range. There is a strong correlation between the directional tuning and the behavioural preference in no-choice tests. This second “matched filter” also varies widely in females, and surprisingly, differs on average by 400 Hz from the neuronal frequency tuning.Conclusions/SignificanceOur findings on the mismatch of the two “matched filters” would suggest that the difference in these two filters appears to be caused by their evolutionary history, and the different trade-offs which exist between sound emission, transmission and detection, as well as directional hearing under specific ecological settings. The mismatched filter situation may ultimately explain the maintenance of considerable variation in the carrier frequency of the male signal despite stabilizing selection.
Highlights
Many acoustic communication systems involve the production and transmission of specific sound frequencies
Our results are compatible with the notion that a matched filter for sound frequency exists in G. bimaculatus, implemented in the receptors of the receiver and read out by the pair of AN1interneurons, which can be considered the ‘‘hard-wired’’ preference function in this insect, since it exhibits a frequency tuning that explains about 80% of the variation in the direction and strength of phonotactic steering in a choice situation
The high correlation between the AN1 threshold differences for different carrier frequency (CF) and the behavior of females in a choice situation indirectly confirm previous results with experimental manipulation of AN1-activity through current injection, which demonstrated that the asymmetric discharge of the pair of AN1-neurons determines the direction of positive phonotaxis [19; 20]
Summary
Many acoustic communication systems involve the production and transmission of specific sound frequencies. The ‘‘matched filter hypothesis’’ [1,2] argues that receivers should gain an advantage from being selectively tuned to these frequencies, in particular in noisy environments, since the match between the sensitivity of their auditory system and the energy spectrum of the senders vocalisation would maximize the signal-to-noise-ratio for reception. Experimental evidence for this hypothesis stems from a comparison of basilar papilla tuning in two populations of cricket frogs, with the population in the acoustically more challenging habitat having evolved a filter that better eliminates noise [3,4]. Individual differences in female preference functions and their proximate causation have rarely been studied
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